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International Journal of
Molecular Sciences
Review
Changes in Photosynthesis Could Provide Important Insight
into the Interaction between Wheat and Fungal Pathogens
Huai Yang and Peigao Luo *
Provincial Key Laboratory for Plant Genetics and Breeding, College of Agronomy,
Sichuan Agricultural University, Chengdu 611130, China; yanghuai202103@163.com
* Correspondence: lpglab@sicau.edu.cn
Abstract: Photosynthesis is a universal process for plant survival, and immune defense is also a
key process in adapting to the growth environment. Various studies have indicated that these
two processes are interconnected in a complex network. Photosynthesis can influence signaling
pathways and provide both materials and energy for immune defense, while the immune defense
process can also have feedback effects on photosynthesis. Pathogen infection inevitably leads to
changes in photosynthesis parameters, including Pn, Gs, and Ci; biochemical materials such as
SOD and CAT; signaling molecules such as H2 O2 and hormones; and the expression of genes in-
volved in photosynthesis. Some researchers have found that changes in photosynthesis activity are
related to the resistance level of the host, the duration after infection, and the infection position
(photosynthetic source or sink). Interactions between wheat and the main fungal pathogens, such as
Puccinia striiformis, Blumeria graminis, and Fusarium graminearum, constitute an ideal study system to
elucidate the relationship between changes in host photosynthesis and resistance levels, based on the
accessibility of methods for artificially controlling infection and detecting changes in photosynthesis,
the presence of multiple pathogens infecting different positions, and the abundance of host materials
Citation: Yang, H.; Luo, P. Changes
with various resistance levels. This review is written only from the perspective of plant pathologists,
in Photosynthesis Could Provide
and after providing an overview of the available data, we generally found that changes in photosyn-
Important Insight into the Interaction
thesis in the early stage of pathogen infection could be a causal factor influencing acquired resistance,
between Wheat and Fungal
while those in the late stage could be the result of resistance formation.
Pathogens. Int. J. Mol. Sci. 2021, 22,
8865. https://doi.org/10.3390/
ijms22168865
Keywords: photosynthesis; wheat diseases; immune defense; ROS; gene expression
Academic Editor: Vitaliy Borisov
Received: 24 July 2021 1. Introduction
Accepted: 13 August 2021 Photosynthesis is a universal process in the plant kingdom that occurs in various green
Published: 18 August 2021 organs, such as leaves [1], young stems [2], green fruits [3], and ears before maturity [4],
providing a material basis and energy supply for multiple physiological metabolic processes
Publisher’s Note: MDPI stays neutral in plants [5]. Plant organs that can perform photosynthesis are considered photosynthetic
with regard to jurisdictional claims in source organs, which mainly include the leaves of plants, while the storage organs of the
published maps and institutional affil-
organic matter synthesized by photosynthesis represent photosynthetic sink organs, which
iations.
include mainly stalks, roots, and fruits [6]. At different growth and development stages, the
photosynthetic sources and sinks can change accordingly. For instance, when plants are in
the seedling stage, leaves and stems act as both sources and sinks of photosynthesis because
photosynthates are supplied for their own growth and development. Photosynthesis is
Copyright: © 2021 by the authors. disrupted by a variety of complex factors, including abiotic stresses caused by water [7],
Licensee MDPI, Basel, Switzerland. temperature [8], light [9], and mechanical damage [10] and biological stresses caused by
This article is an open access article insects and pathogens [11,12]. In contrast, photosynthetic changes during this process may
distributed under the terms and
be related to responses to these factors.
conditions of the Creative Commons
Photosynthesis is sensitive to abiotic stress. Lack of water can limit photosynthesis
Attribution (CC BY) license (https://
efficiency due to thylakoid membrane damage and reduced chlorophyll contents [13].
creativecommons.org/licenses/by/
Both high and low temperatures inhibit the activities of photosynthesis-related enzymes
4.0/).
Int. J. Mol. Sci. 2021, 22, 8865. https://doi.org/10.3390/ijms22168865 https://www.mdpi.com/journal/ijmsInt. J. Mol. Sci. 2021, 22, 8865 2 of 15
and membrane-associated electron carriers, thus further reducing the rate of photosynthe-
sis [14,15]. Light intensities higher than the light saturation point of photosynthesis can
cause photoinhibition of photosystem II (PSII) [9], and limited irradiance also directly leads
to a decline in the photosynthesis rate [16]. In addition, complex photosynthetic changes
can also be caused by the invasion of various insects and pathogens. For example, the
photosynthesis rate of rice leaves is inhibited by Nilaparvata lugens infestation, especially in
the lower part of the leaves [17], and the net photosynthesis rate (Pn) and related param-
eters of susceptible tomato leaves are affected by inoculation with Fusarium oxysporum f.
sp. lycopersici or Verticillium albo-atrum [18]. The photosynthesis capacity of maize leaves
is also inhibited by infection with Colletotrichum musae and Fusarium moniliforme, and the
inhibition is accompanied by a sharp decrease in chlorophyll content [19]. Changes in pho-
tosynthesis in response to changes in environmental conditions constitute a traditional and
interesting topic for scientists in the field of photosynthesis. However, the objective of this
review is to underscore photosynthetic changes during pathogenesis from the standpoint
of pathologists.
It is well known that most pathogen invasions lead to a decline in the photosynthesis
rate of the host [20,21]. However, various authors carefully monitored the photosynthetic
changes during pathogen infection in a host and detected a very significant phenomenon:
in the early stages of infection by a large number of different pathogens, the photosynthesis
capacity of the host always decreases [22–25]. For example, photosynthesis in both resistant
and susceptible barley decreased after inoculation with powdery mildew, and moreover,
the decrease in photosynthesis in the resistant plants was larger than that in the susceptible
plants [22]. Similar decreases were also observed in interactions between tobacco and
Phytophthora nicotianae [23] and between Arabidopsis and Pseudomonas syringae [26]. These
findings indicate that the difference in the degree of photosynthetic changes in the early
stages of infection could conversely be an indicator of the resistance level.
2. Wheat and Its Fungal Pathogens Constitute Ideal Pathogen Systems for Studying
the Role of Photosynthesis in the Process of Resistance Development
2.1. Characteristics of the Three Major Fungal Diseases of Wheat
Wheat is one of the most important crop species and has been a staple food of hu-
mans for thousands of years worldwide [27]. The growth period of wheat is longer than
that of other food crop species such as maize and rice, making wheat more susceptible to
various pathogens and diseases during its growth and development [28]. Among these
diseases, the wheat powdery mildew caused by the obligate biotrophic fungus Blumeria
graminis f. sp. tritici (Bgt), stripe rust caused by the biotrophic parasite Puccinia striiformis f. sp.
tritici (Pst), and Fusarium head blight (FHB), which is caused mainly by Fusarium graminearum
species, are the three most severe diseases affecting both yield and quality [29,30]. The basic
characteristics of the three diseases are listed in Table 1. Wheat powdery mildew is an
epidemic disease worldwide, especially in regions such as southwestern China, whose
environment is temperate and rainy during the wheat growing season [31]. Furthermore,
powdery mildew can occur throughout the whole growth period of wheat, and the optimal
temperature for its occurrence is 15–20 ◦ C [32]. For the infected position, Bgt pathogens
infect mainly the leaves and sometimes also infect green awns, glumes, and stalks [33].
These organs differ largely in the position of the plant, but they are usually considered
photosynthetic source organs at the developmental stage because of their strong photo-
synthetic competence [34]. Therefore, wheat powdery mildew is a typical source disease
from the perspective of photosynthetic function. Wheat stripe rust is also one of the most
threatening diseases in wheat production worldwide [35], especially in temperate climates.
Stripe rust can occur during the whole growth period from seedling emergence to ma-
turity, and the optimum temperature for its occurrence is 13–16 ◦ C [36,37]. The tissue
specificity of stripe rust is stronger than that of wheat powdery mildew, which mainly
parasitizes leaves, the main source of wheat photosynthesis, and seldom occurs in wheat
stems and glumes [38]. Therefore, wheat stripe rust is also a typical source disease from
the perspective of source–sink relationships.Int. J. Mol. Sci. 2021, 22, 8865 3 of 15
Table 1. Characteristics of the three major fungal diseases of wheat.
Major Diseases in Position of Optimal Classification of
Pathogen Infection Period
Wheat Infection Temperature Diseases
Blumeria graminis f.
Powdery mildew leaf whole growth period 15–20 ◦ C [32] source disease
sp. tritici (Bgt)
Puccinia striiformis
Stripe rust leaf whole growth period 13–16 ◦ C [36,37] source disease
f. sp. tritici (Pst)
Fusarium
Fusarium head blight graminearum ear adult stage 20–25 ◦ C [39] sink disease
species complex
It is well known that the occurrence of FHB in wheat is extremely harmful to the quality
of wheat because the causal agent produces the mycotoxin deoxynivalenol (DON), which
is poisonous to both humans and animals [40]. At the same time, FHB can also cause great
loss of wheat yield, especially under the environment conditions suitable for F. graminearum
growth and breeding [41,42]. F. graminearum infects mainly the ears of wheat at the adult
stage, and they are generally considered sink organs due to their role as a storage location
for photosynthates in wheat. Therefore, in contrast to wheat powdery mildew and stripe
rust, FHB is a typical sink disease. Measurements of photosynthesis parameters of FHB-
resistant/susceptible sister-line wheat after inoculation with F. graminearum showed that
the photosynthesis rate of susceptible wheat leaves did not change significantly, while the
photosynthesis rate of resistant wheat leaves decreased significantly in the early stage after
pathogen infection, but the resistant genotype produced a larger yield than the susceptible
genotypes did [43]. This indicates that the decrease in photosynthesis rate could play a key
role in inducing systemic resistance to maintain the ultimate yield.
2.2. Wheat and Its Tissue-Specific Diseases Constitute an Ideal System
The mechanism through which both stripe rust and powdery mildew cause yield
losses could be different from that of FHB because of the difference in the infection positions.
A variety of wheat leaf diseases can reduce the amount of green leaf area, resulting in
a decrease in chlorophyll contents in the infected parts [44], which directly reduces the
photosynthesis capacity and both the synthesis and the accumulation of organic matter in
photosynthetic source organs, leading to a decline in wheat yield [45]. For instance, the
chloroplast envelope of wheat mesophyll cells is disrupted after infection with Bgt, and
the thylakoid becomes enlarged [45]. The effector protein of wheat stripe rust fungus can
inhibit chloroplast function [46], and Pst infection can also reduce the chlorophyll content
in wheat leaves [24]. However, there may be several reasons for wheat yield loss caused
by FHB. Studies have indicated that damaged photosynthetic sink organs may inhibit
photosynthesis at the source via feedback mechanisms, which could be the important
reason to explain the yield loss caused by FHB [43,47].
In addition, a few reports have indicated that photosynthesis may be involved in
wheat immune defense responses to fungal pathogens and may influence resistance forma-
tion because changes in photosynthesis may provide an important signal for maintaining
source—sink balance during interactions between wheat and pathogens [12,48]. However,
there are few relevant research reports on the role of photosynthesis in influencing the
formation of wheat resistance, and those studies have focused mainly on photosynthetic
changes after inoculation with pathogens, so knowledge about the influence of photosyn-
thesis is very fragmented or not systematic [49]. Both wheat powdery mildew and stripe
rust are source organ diseases, and FHB is a sink organ disease. Hence, wheat and its fungal
pathogens constitute an ideal pathogen system for exploring the role of photosynthesis in
the development of wheat resistance.Int. J. Mol. Sci. 2021, 22, 8865 4 of 15
3. Relationships between Yield and Photosynthetic Changes Caused by Pathogen
Infection in Wheat
3.1. Effects of Photosynthetic Changes on Wheat Yield
Decreases in wheat yield caused by pathogen infection have always been a focus of
wheat breeders and physiologists [50]. A large number of studies have reported adverse
effects of wheat leaf diseases (such as powdery mildew and stripe rust) and ear diseases
(such as FHB) on wheat yield [51,52]. Infection of wheat powdery mildew at the seedling
stage can affect the growth and development of wheat plants [53] and can further lead
to a decrease in grain filling and grain weight at the adult stage [33]. Wheat stripe rust
infection not only can reduce the number of tillers at the tillering stage [54] but also
can significantly reduce the grain number per spike and 1000-grain weight at the adult
stage [55]. Wheat stripe rust and powdery mildew have very similar effects on wheat yield
because they both directly act on the source organs of wheat photosynthesis and cause
wheat yield losses through long-term inhibition of photosynthesis in wheat leaves [52,56,57].
In addition, both Bgt and Pst are parasitic fungi that rely on host metabolism to provide
carbohydrates, amino acids, and inorganic nutrients [58,59]. The growth and reproduction
of a large number of pathogens directly consume nutrients in photosynthetic source organs,
further reducing wheat yields [58].
The production of the mycotoxin DON in diseased wheat ears is the main negative
effect caused by FHB but could also lead to severe yield losses due to a damaged photosyn-
thetic sink and a disrupted source–sink balance [40,43]. It has been reported that FHB can
cause 10–70% yield losses in years in which epidemics occur [45]. Unfortunately, how the
damage of photosynthetic sink organs causes the changes of photosynthetic source organs
remains to be further explored. It has been reported that the activity of photosynthesis-
related enzymes and the expression of associated gene transcripts are modified by sink
demand [60]. Stomatal closure is a plant’s first line of defense against pathogens [61].
Recent studies have suggested that the reduced photosynthetic efficiency of susceptible
wheat leaves is regulated by stomatal factors after the occurrence of FHB symptoms, while
the Gs of resistant wheat leaves did not show a significant decrease under the same treat-
ment [43,50]. These reports suggest that when pathogens attack the photosynthetic sinks
of wheat, there is some kind of feedback regulatory mechanism that alters the balance
between photosynthetic sources and sinks by adjusting photosynthesis parameters.
3.2. Association between Changes in Photosynthesis and Immune Defense in the Early Stages after
Pathogen Infection
In the past, plant defense responses and photosynthesis have been studied inde-
pendently. With the mechanisms underlying plant photosynthesis and immune defense
gradually becoming clear, it has been found that plant photosynthesis can provide materi-
als and can serve as a signal transduction basis for plant immune defense [49,62], which
indicates that plant photosynthesis and immune defense processes are interconnected [63].
A series of reports have shown that host photosynthesis usually declines in the early stages
of invasion by various pathogens [25,64–66], which may be involved in the immune re-
sponse of the host. For instance, in incompatible reactions between tobacco and P. nicotianae,
the photosynthetic electron transport chain in tobacco leaves is disrupted, and photosyn-
thetic activity decreases with the accumulation of reactive oxygen species (ROS) just a
few hours after inoculation [23]. Moreover, when interactions between Arabidopsis and
P. syringae strains were analyzed, it was found that both virulent and avirulent strains of
P. syringae could cause a decrease in photosynthesis in Arabidopsis leaves, and a decrease
in photosynthesis was detected within only 3 h after pathogen inoculation during incom-
patible reactions [24]. Although the molecular mechanism underlying the decrease in
photosynthesis caused by pathogen infection in the early stage remains unclear, recent
studies on photosynthetic changes caused by various pathogens have provided several
clues to help elucidate the role of photosynthetic changes in the defense response.Int. J. Mol. Sci. 2021, 22, 8865 5 of 15
Infection of wheat pathogenic fungi in the leaves and ears can cause a decrease in
photosynthesis in wheat leaves. The decline in photosynthesis in the early stage of various
fungal pathogens invasion in wheat are listed in Table 2. In incompatible reactions, the
decrease in photosynthesis capacity of the host may be due to the material and energy
needed for defense [67], while in compatible reactions, the decrease in photosynthesis
capacity may be due to the damage caused by pathogen infection of the host [68,69]. Unlike
the transcriptomic and photosynthetic changes in sister wheat lines after inoculation with
Bgt., it was found that the inhibition of photosynthesis in resistant wheat paralleled the
global downregulation of photosynthesis-related genes to actively regulate the immune
response, but the decrease in photosynthesis in susceptible wheat lines is caused by stom-
atal closure and did not regulate the immune response [25]. The infection of wheat stripe
rust also causes a phenomenon similar to that caused by powdery mildew. The Pn of the
resistant cultivar CN19 carrying the gene Yr41 [70] and the susceptible cultivar Sy95-71
decreased significantly at 72 h after inoculation with Pst compared with no inoculation [24].
By exploring the resistance mechanism of wheat resistance genes, it was also found that,
by inhibiting photosynthesis, the stripe rust resistance gene Yr36 could provide broad-
spectrum resistance to Pst races in wheat at the adult stage [71]. Studies on the signals of
photosynthetic changes caused by wheat leaf diseases have also suggested that the resistant
genotypes of wheat could actively regulate photosynthetic changes to mediate specific
immune defenses against the invasion of pathogens, albeit at a cost of greatly reduced
photosynthesis capacity in the initial stage of pathogen infection [72]. Taken together, these
results indicate that the changes in photosynthesis parameters in the early stage of stripe
rust and powdery mildew infection in wheat were related to the development of resistance.
Table 2. Changes in photosynthesis and antioxidant enzyme activity in response to the three main fungal pathogens in
wheat at the early stage of infection (within 72 h).
Major Diseases Wheat
Parameter (Leaf) Resistance 0h 12 h 24 h 48 h 72 h
in Wheat Cultivar/Line
Powdery mildew Pn [25] L658 R CG & % → &
L958 S CG & % → &
SOD [25] L658 R CG → → → &
L958 S CG % → & &
CAT [25] L658 R CG & % & %
L958 S CG → % & &
Stripe rust Pn [24] CN19 R CG – – – &
Sy95-71 S CG – – – &
psbo-A1
Pn [73] R – – – & –
Mutant
Kronos S – – – CG –
Fusarium head blight Pn [74] L693 R CG – & → →
L661 S CG – → → →
SOD [74] L693 R CG – & → →
L661 S CG – % → →
CAT [74] L693 R CG – % → →
L661 S CG – & & &
CP: control group; &: indicates that the current time has decreased significantly from the previous point in time; %: indicates that current
time has increased significantly from the previous point in time; →: indicates that current time had no significant change from the previous
point in time; –: indicates that no available data were detected.
Interestingly, photosynthesis-related parameters in the ears and leaves of resistant
and susceptible wheat were found to be significantly different after inoculation with
F. graminearum [74]. The photosynthesis of wheat spikes increased at the early stage of
inoculation in both resistant and susceptible plants, although the spikes were directly
infected by F. graminearum; however, there was a larger increase in the ears and a larger
decrease in the leaves in the resistant plants than in the susceptible plants [74]. Therefore,Int. J. Mol. Sci. 2021, 22, 8865 6 of 15
changes in the photosynthesis parameters of different genotypes of wheat may provide
important insight into the mediation of immune defense responses to wheat sink diseases.
4. ROS Produced by Photosynthesis Relay Compatibility or Incompatibility Signals
Photosynthesis can regulate the immune defense response in many ways, the most
important of which is by inducing the production of ROS and regulating changes in hor-
mones [12,48,67]. ROS, including singlet oxygen (1 O2 ), superoxide anion radicals (O2•− ),
hydrogen peroxide (H2 O2 ), and hydroxyl radicals (•OH) are produced mainly during
interactions between metabolic intermediates and oxygen during photosynthesis [75,76].
The concentration of ROS in plants is maintained usually at low levels due to rapid and
precise regulation by various antioxidant enzymes, mainly catalase (CAT), superoxide
dismutase (SOD), ascorbate peroxidase (APX), and peroxidase (POD) [76]. The metabolism
of ROS has a dual role in plant growth and development. On the one hand, high concen-
tration of ROS accumulation in plant cells can ultimately damage proteins, lipids, and
nucleic acids and can even disrupt photosynthesis, and ROS are toxic to many cellular
processes in plants [77–79]. On the other hand, a role for ROS in the immune defense
has gradually been elucidated, indicating that ROS play a crucial role in plant immune
defense [80]. The production of ROS is one of the earliest cellular reactions following
pathogen recognition [81]. Many studies have revealed that low concentrations of ROS can
activate the expression of defense-related genes and induce various defense responses [82],
while a high accumulation of ROS can be used as a defense weapon to resist pathogen
invasion [83]. In addition, ROS can regulate immune defense through interactions with
plant hormones [84,85], and the synergistic effect of ROS and salicylic acid (SA) plays
an important role in mediating the hypersensitive response (HR) [86,87]. In interactions
between plants and pathogens, the ROS that accumulate are generated mainly by photosys-
tem I (PSI) and PSII during photosynthesis [88]. Therefore, the changes in ROS caused by
photosynthetic changes could be an important factor explaining why early photosynthesis
is involved in the development of plant disease resistance, which ultimately results in
compatibility or incompatibility between pathogens and hosts.
A large number of studies have suggested that the accumulation of ROS, particularly
H2 O2 , constitutes an important signal that is transmitted and may determine the compati-
bility between pathogenic fungi and wheat in the early stage of infection [69,73,89]. For
instance, transgenic experiments confirmed that, after being transferred to a resistance
gene, the powdery mildew resistance of susceptible wheat variety Yangmai 158 was sig-
nificantly improved at the seedling and mature stages and accumulated more ROS at the
Bgt infection position [90]. The results indicate that ROS could improve the resistance
of wheat to powdery mildew. By measuring the changes in ROS and photosynthesis in
resistant/susceptible sister wheat lines after inoculation with Bgt, Hu et al. [25] reported
that two stages of H2 O2 bursts occurred during the incompatible reaction process and that
a single low-amplitude and transient H2 O2 outbreak in susceptible wheat lines was not
sufficient to induce the HR. In addition, ROS signaling plays a crucial role in the immune
response to stripe rust caused by the parasitic fungus Pst. Overexpression of LSD-1-like
zinc-finger protein (TaLOL), which actively regulates the ROS signaling pathway, can en-
hance resistance to stripe rust by inducing the production and accumulation of ROS and
cell death, while silencing TaLOL2 increases sensitivity to avirulent races of Pst and reduces
ROS production in wheat [73]. These results indicate that the accumulation of ROS acts as
an important signal of immune defense in wheat leaf diseases caused by parasitic fungi.
FHB resistance is an extremely complex trait that is controlled by multiple quantitative
trait loci (QTLs) and includes the additive effect of several genes [91]. Wheat resistance
to FHB consists of two main types: resistance to the initial infection (type I resistance)
and resistance to the spread of the disease within the wheat head (type II resistance) [92].
F. graminearum, the causal agent of wheat FHB, is a hemibiotroph that can absorb nutrients
from dead tissues, so the HR mediated by the accumulation of ROS may not easily effec-
tively resist FHB [93]. The results of some studies on the changes in ROS levels duringInt. J. Mol. Sci. 2021, 22, 8865 7 of 15
FHB infection are consistent with our views. For instance, comparative transcriptome
analysis suggested that ROS may accumulate in susceptible mutants of the wheat cultivar
Wangshuibai after inoculation with F. graminearum but not in FHB-resistant cultivars of
Wangshuibai [94]. Another example is the FHB-resistant line L693, which exhibits tempo-
rary infection symptoms due to insufficient accumulation of ROS after inoculation with
F. graminearum, after which systemic acquired resistance (SAR) is induced in distal tissues
via the SA pathway to resist pathogen invasion [74]. These results indicate that type
II resistance to spreading within the wheat head mediated by the jasmonic acid (JA) or
SA pathway may determine the compatibility between pathogens and wheat instead of
mediating a strong immune defense response based on ROS at the site of parasitic fungal in-
fection [74,94,95]. Therefore, it is difficult to determine the compatibility of F. graminearum
with wheat by outbreak of ROS in the infected position, but ROS produced in a pathogen-
infected position may play a role in signaling pathways because ROS are closely related to
the SA pathway.
5. Gene Expression Change Profiles Support the View That Photosynthesis Plays an
Important Role in the Formation of Resistance
The changes in photosynthesis parameters, ROS bursts, and POD activity during
compatibility and incompatibility responses can reveal only superficial changes in the
plant-mediated immune defense response. The gene expression change profiles in the inter-
action between pathogens and host can systematically reveal the changes of physiological
metabolism and signaling molecules involved in immune defense during the formation
of host resistance [96–98]. During pathogen invasion, the changes of host photosynthesis
were associated with the expression of photosynthesis-related genes [99]. The expression
of genes related to the regulation of ROS and plant hormone synthesis and catabolism
can indicate the changes of ROS and hormone levels in the host [100]. For instance, some
studies have indicated that the expression of photosynthesis-related genes is generally
downregulated under biotic stress, which is conducive to the production of ROS [101,102],
while the upregulated expression of genes involved in the synthesis of JA, SA, and ethy-
lene (ET) can stimulate the hormone-mediated defense response [103]. In addition, the
accumulation of H2 O2 in chloroplasts can lead to an increase in the level of SA [104], which
in turn inhibits H2 O2 -scavenging enzymes such as CAT and APX [105]. In the process
of interaction between host and pathogen, ROS, antioxidant enzymes, plant hormones,
and photosynthesis constitute a complex mutual regulation network, and it is difficult to
explore the relationship between them only by measuring physiological and biochemical
indicators [106,107]. Therefore, comparing the changes in photosynthesis-related genes
during the occurrence of different types of fungal diseases in wheat is beneficial for un-
derstanding the molecular mechanism through which wheat mediates different types of
immune defense processes.
5.1. Global Downregulation of Photosynthesis-Related Genes in Response to Many Wheat Diseases
May Disrupt Photosynthesis and Promote ROS Production
ROS, mainly H2 O2 , are key immune defense products of photosynthesis [84,108,109].
In incompatible reactions, the accumulation of ROS is usually accompanied by a decrease
in the photosynthesis rate because the inhibition of photosynthesis is conducive to ROS
production and accumulation [110,111]. Moreover, pathogens invasion usually results
in the downregulation of photosynthesis-related genes in the host even if the host is not
sensitive to the pathogen [65,112]. These findings indicate that active downregulation of
photosynthesis-related genes in incompatible reactions can induce the accumulation of
ROS, driven by a decrease in the photosynthesis rate of the host. This idea is supported by
numerous reports of changes in the expression of photosynthesis-related genes caused by
interactions between wheat and its pathogens [113–115]. For example, RNA sequencing of
wheat infected by Bgt revealed that ROS bursts are accompanied by a global downregula-
tion of photosynthesis-related genes, including those encoding chlorophyll a/b-binding
(Cab) protein, ribulose bisphosphate carboxylase small chain (RbcS) protein, and ATPInt. J. Mol. Sci. 2021, 22, 8865 8 of 15
synthase, which parallel the decrease in the Pn [25]. Moreover, the significant decrease
of chlorophyll fluorescence parameters (Fv’/Fm’, Fv/Fm, ΦPSII, ETR, qP) indicated that
the photosynthetic electron transport chain of resistant wheat was blocked at the early
stage of Bgt inoculation, which further supported that the decrease of photosynthesis was
related to ROS production [25]. Transcriptome analysis of the susceptible cultivar Jingdong
8 and its resistant near-isogenic line also showed that the expression of a large number
of photosynthesis-related proteins was inhibited at the early stage of inoculation with
Bgt [116]. Additionally, the WKS1 protein encoded by stripe rust resistance gene Yr36
can phosphorylate an extrinsic member of PSII and reduce photosynthetic rate [71]. In
addition, comparison of the gene expression profiles of resistant wheat after inoculation
with Pst revealed that the systems that produce ROS and nitric oxide (NO) are enriched,
and the expression of photosynthesis-related genes is also reduced during this period [114].
Taken together, these results support the idea that active downregulation of photosynthesis-
related genes disrupts photosynthesis as part of the incompatibility between parasitic fungi
and wheat, which is associated with the activation of immune defenses.
Associations between F. graminearum infection and changes in photosynthesis in wheat
have not been consistently recognized. Multiple gene expression profiles of FHB infection
have suggested that the regulation of photosynthesis-related genes involving resistance
to FHB is quite different from that involving stripe rust and powdery mildew. For exam-
ple, analysis of the gene expression profile of QTL FhbL693b, which is a genomic region
associated with FHB resistance, revealed that most of the differentially expressed genes
detected in the region were related to photosynthesis, which indicates that photosynthe-
sis may be involved in FHB resistance [74]. In addition, integrative transcriptome and
hormone analysis indicated that SA and JA played a positive role in FHB resistance and
that photosynthesis-related genes of the resistant variety Sumai 3 were downregulated
at the early stage of inoculation [97]. Another study suggested that the ROS signaling
pathways mediated by photosynthesis-related genes were not extremely important in FHB
resistance because ROS-producing/scavenging systems were more active in the suscep-
tible mutant than in the resistant variety Wangshuibai [94]. What is more, the transient
susceptibility of the FHB-resistant line L693 and the inhibition of the ROS production sys-
tem in Wangshuibai after inoculation indicated that photosynthesis-related genes did not
directly induce the production of ROS to mitigate FHB resistance [74,94]. The development
of resistance to FHB in wheat may depend on the activation of SAR by the SA and JA
signaling pathways [97], which is also related to photosynthesis due to the synthesis of
related hormones, mainly in chloroplasts [117].
5.2. Photosynthesis-Related Genes Directly Regulate the Immune Defense
In addition to producing ROS and regulating plant hormone levels to indirectly partic-
ipate in plant immune defense, some proteins related to photosynthesis and genes related
to photorespiration can directly regulate the defense response [118,119]. For example,
the electron receptor protein ferredoxin-I (FD-I), which is involved in the photosynthetic
process, is closely related to the production of ROS and the induction of the HR [120].
Inducing ferredoxin-like protein (AP1) expression in transgenic rice can increase resis-
tance to Xanthomonas oryzae pv. oryzae [121]. In addition, compared with their wild-type
counterparts, transgenic lines of Oncidium orchids are more resistant to soft rot disease
when the coding sequence of ferredoxin-like protein (pflp) is transfected [122]. Moreover,
transient overexpression of glycolate oxidase (GOX2), serine glyoxylate aminotransferase (SGT),
and serine hydroxyl methyltransferase (SHMT1), which are involved in photorespiration in
tobacco, increased the basic defense of transgenic lines against P. syringae [118]. On the
other hand, interactions between pathogens and hosts revealed that many fungal effectors
directly acted on chloroplasts and inhibited the immune response of plants by affecting the
function of chloroplasts so that pathogens could successfully invade the host [20,123,124].
These clues suggest that several resistance genes may function together with photosynthesis
to resist pathogen invasion.Int. J. Mol. Sci. 2021, 22, 8865 9 of 15
Changes in the expression of photosynthesis-related genes in wheat during pathogen
invasion and photosynthetic changes caused by wheat resistance genes can help to com-
pensate for the gaps in knowledge concerning the mechanisms underlying resistance genes
in wheat. Lots of studies have indicated that the development of resistance through the
action of several wheat resistance genes relies on photosynthesis and chloroplasts [125–127].
For instance, to improve wheat powdery mildew resistance, the transfection of several
receptor protein kinase-encoding genes can improve resistance to powdery mildew by
inducing ROS bursts [90,126,127]. A recent discovery showed that protein kinase recep-
tors could phosphorylate NADPH oxidase to activate ROS in Arabidopsis thaliana, which
implies that there is a link between resistance genes of receptor protein kinase and pho-
tosynthesis in wheat [126,128,129]. In addition, the wheat stripe rust resistance protein
WKS1 directly phosphorylates thylakoid-associated ascorbate peroxidase (TAPX) in chloro-
plasts and decreases its peroxide-scavenging ability [130]. The WKS1 also acts directly in
chloroplasts to participate in immune defense responses. Moreover, Li et al. [74] identified
three photosynthesis-related genes involved in the development of FHB resistance via
transcriptome analysis in the chromosomal region of the resistance QTL FhbL693B [74].
Together, these reports show that photosynthesis plays a key role in wheat resistance and
that wheat resistance genes may regulate photosynthesis to mediate resistance against
pathogen invasion.
6. Summary and Future Efforts
Similar to how temperature can be an indicator of disease for a doctor, photosynthesis
could be an important indicator for a plant pathologist speculating about the results of
interactions between hosts and pathogens. Changes in photosynthesis parameters in the
early stage (usually within 24 h) after pathogen infection could be an important causal
agent contributing to the final resistance ability of plants, while changes in the late stage
(usually 72 h) after pathogen infection could be the result of the resistance response. In
addition, wheat and its main fungal pathogens, including Bgt, Pst, and F. graminearum,
constitute ideal plant–pathogen systems because of their different infection positions from
a photosynthetic standpoint. By providing an overview of the relevant data, we aimed
to develop a model to explain the putative mechanism through which photosynthesis is
involved in the wheat resistance response (Figure 1). Infection with source pathogens could
cause a decrease in the photosynthesis rate, while infection with sink pathogens could
lead to an increase in the photosynthesis rate at local infection positions, but both infection
types directly and indirectly result in a decrease in the photosynthesis rate in source
organs, which may be associated with SAR. Usually, the larger the decreased amplitude
is, the greater the tendency of incompatibility. This could be explained in view of the
accumulation of ROS, especially H2 O2 , in source organs, which could be further used as
signaling molecules to activate the HR and SAR. In our opinion, a clearer relationship
or defined role of photosynthesis in interactions between hosts and pathogens could be
determined by additional solid evidence in the future.Int. J. Mol. Sci. 2021, 22, 8865 10 of 15
Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 10 of 15
Figure1.1.Hypothesized
Figure Hypothesizedmodel
modelofofphotosynthesis
photosynthesisinvolving
involvinginformation
informationconcerning
concerningresistance
resistancetoto
wheat source and sink diseases in the early stages of pathogen invasion.
wheat source and sink diseases in the early stages of pathogen invasion.
AuthorContributions:
Author Contributions:P.L.P.L.formulated
formulatedthe
theconcept
conceptofofthe
thereview;
review;H.Y.
H.Y.wrote
wrotethe
thedraft;
draft;P.L.
P.L.cowrote
cowrote
and edited the draft; H.Y. prepared the figures. All authors have read and agreed to the published
and edited the draft; H.Y. prepared the figures. All authors have read and agreed to the published
versionofofthe
version themanuscript.
manuscript.
Funding:This
Funding: Thisresearch
researchreceived
receivedno
noexternal
externalfunding.
funding.
InstitutionalReview
Institutional ReviewBoard
BoardStatement:
Statement:Not
Notapplicable.
applicable.
InformedConsent
Informed ConsentStatement:
Statement:Not
Notapplicable.
applicable.
DataAvailability
Data AvailabilityStatement:
Statement:Not
Notapplicable.
applicable.
Acknowledgments:We
Acknowledgments: Weareare grateful
grateful to the
to the reviewers
reviewers for their
for their comments
comments and suggestions
and suggestions on thison this
review.
review.
Conflicts of Interest: The authors declare that they have no conflicts of interest.
Conflicts of Interest: The authors declare that they have no conflicts of interest.
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